Ecosystems are being altered on a global scale by the extirpation of top predators. The ecological effects of predator removal have been investigated widely; however, predator removal can also change natural selection acting on prey, resulting in contemporary evolution. Here we tested the role of predator removal on the contemporary evolution of trophic traits in prey. We utilized a historical introduction experiment where Trinidadian guppies (Poecilia reticulata) were relocated from a site with predatory fishes to a site lacking predators. To assess the trophic consequences of predator release, we linked individual morphology (cranial, jaw, and body) to foraging performance. Our results show that predator release caused an increase in guppy density and a “sharpening” of guppy trophic traits, which enhanced food consumption rates. Predator release appears to have shifted natural selection away from predator escape ability and towards resource acquisition ability. Related diet and mesocosm studies suggest that this shift enhances the impact of guppies on lower trophic levels in a fashion nuanced by the omnivorous feeding ecology of the species. We conclude that extirpation of top predators may commonly select for enhanced feeding performance in prey, with important cascading consequences for communities and ecosystems.
The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar-built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re-form within a few weeks or months, thereby re-isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within-population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes Eda and Pitx1 and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among-population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within-population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype and the presence of predators, thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within-population variation while reducing, but not eliminating, among-population variation driven by spatial environmental variation.
Parallel evolution is considered strong evidence for natural selection. However, few studies have investigated the process of parallel selection as it plays out in real time.The common approach is to study historical signatures of selection in populations already well adapted to different environments. Here, to document selection under natural conditions, we study six populations of threespine stickleback (Gasterosteus aculeatus) inhabiting bar-built estuaries that undergo seasonal cycles of environmental changes. Estuaries are periodically isolated from the ocean due to sandbar formation during dry summer months, with concurrent environmental shifts that resemble the long-term changes associated with postglacial colonization of freshwater habitats by marine populations. We used pooled whole-genome sequencing to track seasonal allele frequency changes in six of these populations and search for signatures of natural selection. We found consistent changes in allele frequency across estuaries, suggesting a potential role for parallel selection. Functional enrichment among candidate genes included transmembrane ion transport and calcium binding, which are important for osmoregulation and ion balance. The genomic changes that occur in threespine stickleback from bar-built estuaries could provide a glimpse into the early stages of adaptation that have occurred in many historical marine to freshwater transitions.
Ecosystem size is known to influence both community structure and ecosystem processes. Less is known about the evolutionary consequences of ecosystem size. A few studies have shown that ecosystem size shapes the evolution of trophic diversity by shaping habitat heterogeneity, but the effects of ecosystem size on antipredator trait evolution have not been explored. Ecosystem size may impact antipredator trait evolution by shaping predator presence (larger ecosystems have longer food chains) and habitat complexity (larger ecosystems may have more diverse habitat structure). We tested these effects using threespine stickleback from bar‐built estuaries along the Central Coast of California. These stickleback populations are polymorphic for Ectodysplasin‐A (Eda), a gene that controls bony lateral plates used as antipredator defense. We inferred Eda genotypes from lateral plate phenotypes and show that the frequency of the complete (C) allele, which is associated with greater number of lateral plates, increases as a function of ecosystem size. Predator presence and habitat complexity are both correlated to ecosystem size. The strongest proximate predictor of Eda allele frequencies was the presence of predatory fishes (steelhead trout and sculpin). Counter to expectations, habitat complexity did not have a strong modifying effect on Eda allele frequencies. Our results point to the importance of ecosystem size for determining predator presence as being the primary pathway to evolutionary effects. Ecosystem size has received much attention in ecology. Our work shows that it may be an important determinant of adaptive evolution in wild populations.
The ability to move between habitats has important implications for fitness in many species. In‐stream barriers such as culverts can impede movements of riverine fishes and thus reduce connectivity between habitats. The ability of fish to overcome barriers is related to the features of the environment and the barrier itself, but also to physiological, morphological and behavioural traits of the fish. Among these, body shape varies among and within species, and influences swimming ability, a key component of passage performance through culverts. We conducted an experimental study on wild brook trout (Salvelinus fontinalis) to assess the effects of individual body shape on attempt rate and passage success through culverts on six streams. A more streamlined body shape was associated with an increased motivation to enter and ascend the culverts, and, to a lesser extent, with the probability of successful passage once an attempt was staged. Motivation and successful passage were also influenced by the density of conspecifics below the culvert, time of day, fish body size and water velocity. Policy implications. While fish body shape is expected to influence swimming performance, our research shows the most important effect of body shape to be on an individual's motivation to stage passage attempts at culverts. This study points to an important connection between behaviour and morphological traits that influence passage success and suggests that in‐stream barriers may be an important agent of selection on behaviour and morphology in wild fish populations.
Fluctuations in the population abundances of interacting species are widespread. Such fluctuations could be a response to abiotic factors, biotic interactions, or a combination of the two. Correctly identifying the drivers is critical for effective population management. However, such effects are not always static in nature. Nonlinear relationships between abiotic factors and biotic interactions make it difficult to parse true effects. We used a type of nonlinear forecasting, empirical dynamic modeling, to investigate the context‐dependent species interaction between a common fish (three‐spine stickleback) and an endangered one (northern tidewater goby) in a fluctuating environment: a central California bar‐built estuary. We found little evidence for competition, instead both species largely responded independently to abiotic conditions. Stickleback were negatively affected by sandbar breaching. The strongest predictor of tidewater goby abundance was stickleback abundance; however, this effect was not a uniform negative effect of stickleback on goby as would be hypothesized under interspecific competition. The effect of stickleback on gobies was positive, though it was temporally restricted. Tidewater goby abundance in the summer was strongly positively correlated to stickleback abundance in the spring, which represents an offset in the reproductive and recruitment peaks in the two species that may help minimize competition and promote coexistence. Our study demonstrates how empirical dynamic modeling can be applied to understand drivers of population abundance in putative competitors and inform management for endangered species.
Transgenerational plasticity (TGP) occurs when phenotypes are shaped by the environment in both the current and preceding generations. Transgenerational responses to rainfall, CO 2 and temperature suggest that TGP may play an important role in how species cope with climate change. However, little is known about how TGP will evolve as climate change continues. Here, we provide a quantitative test of the hypothesis that the predictability of the environment influences the magnitude of the transgenerational response. To do so, we take advantage of the latitudinal decrease in the predictability of temperatures in near shore waters along the US East Coast. Using sheepshead minnows ( Cyprinodon variegatus ) from South Carolina, Maryland, and Connecticut, we found the first evidence for a latitudinal gradient in thermal TGP. Moreover, the degree of TGP in these populations depends linearly on the decorrelation time for temperature, providing support for the hypothesis that thermal predictability drives the evolution of these traits.
Natural selection shapes the evolution of antipredator traits in prey. However, selection in the wild depends on ecological context, including features of predator and prey populations, making field studies of selection critical to understanding how predators shape selection on prey defences. Threespine stickleback (Gasterosteus aculeatus) is a classic system to study the effects of predators on the natural selection of prey.In lakes and rivers, fish predators have been shown to impose selection against low plated adult stickleback phenotypes and genotypes. We directly measured selection by predatory salmonids on the Ectodysplasin-A (Eda) gene in estuary stickleback from California. Despite previous studies showing a positive correlation between predator presence and frequency of the Eda "complete" allele in estuary populations, we found that Eda "low" genotypes were not significantly more frequent in salmonid predator diets. Further, we found no evidence of changes in Eda genotype frequencies across generations that would suggest directional selection driven by predators. Prior selection studies have examined the effects of large resident trout on adult stickleback. In contrast, predators in this study were juvenile anadromous salmonids, which only ate juvenile stickleback whose plate phenotypes had not fully developed. Thus, in this case, predator life history and stickleback ontogeny may preclude strong selection on stickleback armour. Our results underscore the importance of selection studies in the wild for understanding the context-dependent nature of selection in natural populations.
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